Iguana melanoderma, Breuil & Schikorski & Vuillaume & Krauss & Morton & Corry & Bech & Jelić & Grandjean, 2020

Breuil, Michel, Schikorski, David, Vuillaume, Barbara, Krauss, Ulrike, Morton, Matthew N., Corry, Elizabeth, Bech, Nicolas, Jelic, Misel & Grandjean, Frederic, 2020, Painted black: Iguana melanoderma (Reptilia, Squamata, Iguanidae) a new melanistic endemic species from Saba and Montserrat islands (Lesser Antilles), ZooKeys 926, pp. 95-131 : 95

Iguana melanoderma sp. nov. Figures 5 , 6 , 7

Diagnosis.

A species of Iguana , with a distinctive melanistic phenotype, with a black dewlap, huge tubercular nape scales, the absence of horns on the snout.

Etymology.

The name was chosen to emphasize the most conspicuous feature of this new taxon, from melano meaning black and derma meaning skin.

Common local names are: Melanistic Lesser Antilles iguana , Saban Black iguana

Type material.

Choice of the holotype and the paratype. The choice of our type specimens and the way we conducted the description of the type and the paratype attempt to best meet the criteria proposed by ( Dubois 2009) for the case of Conolophus marthae described by Gentile and Snell (2009). We took into account the same kind of problems of sacrificing a specimen for museum collection and referencing an emblematic, iconic, large lizard that belongs to an endangered taxon.

(1) The Saba and Montserrat populations survived for a long time in a period when the risk of extinction was lower than today. Nevertheless, the iguanas were hunted for food, killed by cats and dogs, and their habitats destroyed by livestock and natural events. Today, in Saba, the main risk for this small endemic population, which seems to be far from the carrying capacity of the island, is the arrival of invasive common iguanas from South and Central America that have a rapidly expanding population in Saint Maarten. In Montserrat, the same risk exists. Volcanic eruptions are also a major threat to these populations, as evidenced by the eruption of the Soufrière Hills in Montserrat in 1995 and the following years, which destroyed about a third of the island.

Hybridization with closely related lineages may in-fact be the greatest risk and could very likely lead to extinction of endemic lineages, as is the case for Iguana delicatissima in Guadeloupian Archipelago ( Vuillaume et al. 2015). Moreover, the description of a new taxon may attract collectors and lead to unintended and undesirable consequences. This is of concern because on the Dutch island of Saint Maarten, both the legal and illegal pet trades are common. With the description of this new taxon, local authorities, such as the Saba Conservation Foundation and the NGO Sea and Learn, will have tools to protect the Saban Black Iguana from poaching on an island where the terrestrial protected area is less than 0.5 sq. km on the edge of this endemic iguana 's range.

(2) Lazell (1973) studied and collected iguanas in Saba and Montserrat in the 1960s. The vouchers are deposited at the Museum of Comparative Zoology (Harvard) with two other individuals collected in the seventies. Six vouchers for these two islands (Saba: MCZ R-75832, R-75833, R 133096; Montserrat: MCZ: R-61119, R-82310, R-126377) are present but unfortunately it is almost impossible to measure them properly due to their poor condition. In addition, some are young individuals, which do not have well developed diagnostic characteristics.

(3) We have no precise idea of the size of the iguana population in Saba and Montserrat. Rough estimates based on density in some surveyed areas yield 100-300 adults and subadults for each island. In theory, it is always possible to catch a senile non-breeding male and prepare it in good conditions act as a voucher that will be available in a Museum collection for future study. But, for technical reasons, when the first author was in Saba in 2012, it was not possible to collect such an individual. Roadkill animals are often in poor conditions (broken, flattened, rotten) and in most cases cannot be studied and preserved in a zoological reference collection. The same remarks apply to the Montserrat population.

(4) Since diagnostic characteristics are mainly visible in adult individuals and are not measurements, we chose for the holotype of this new taxon specimen MCZ R-75032 from Saba collected by JD Lazell 6/23/63 on the Windward side of Saba. The paratype MCZ R-126377 is a head of an adult from Montserrat collected by JO Boos at Old Road Bluff 8/6/1970. These two samples are housed at the Museum of Comparative Zoology (MCZ, Harvard). They present the diagnostic characters as described by ( Breuil 2013, 2016) and represent the populations of the two islands, respectively.

Holotype

(Fig. 5 ). Lesser Antilles, Saba• ♀; Windward side; 23 June 1963; JD Lazell [leg.]; MCZ (R-75832).

This individual from Saba was not measured in detail because of the risk of spoiling the specimen. It is an adult female of approximately 26.3 cm SVL and a tail length of approximately 66.4 cm and a total length of 92.7 cm (measurements and photographs by Joseph Martinez, MCZ, Harvard).

Description of the holotype.

The subtympanic plate is round, with a dark patch in the posterior part. The anterior, upper, and lower parts of the subtympanic plate are surrounded by black pigment. Most labial and sublabial scales have dark coloration on their anterior side. The lower labial scales, before the subtympanic plate, are arranged in a series of five pairs of scales of quite similar size and located one in front of the other. The tubercular nape scales are numerous, well developed, grey, and aligned in rows.

Color pattern.

This specimen is partially discolored, with a slight carpet pattern, the stripes on the tail are almost invisible in the photographs, but according to ( Lazell 1973) who captured this specimen, it had a conspicuous carpet pattern.

The dewlap is black in its lower part, and there are nine small, triangular yellowish gular spikes. The tympanum is brown. There is a conspicuous black spot between the eye and the tympanum. The snout and the top of the head are light, not black. The dorsal spikes are greenish and black.

Paratype

(Fig. 6 ). Lesser Antilles, Montserrat • ♂; Old Road Bluff; 6 Aug. 1970; JO Boos [leg.]; MCZ R-126377.

Description of the paratype.

This individual is only a head of a small adult male based on the size of the dorsal spikes. This head presents the typical characteristics of this taxon: large grey scales on the tubercular nape, black spot between the eye and the tympanum, and labial and sublabial scales with black patches on the anterior part. There are five pairs of scales before the subtympanic plate almost completely black, a black dewlap, and a flat head with a light snout (photographs by Joseph Martinez, MCZ Harvard).

Type locality.

On the Windward side of Saba for the holotype and on Old Road Bluff, west coast of Montserrat for the paratype (Figs 1 , 11 ).

Description of Iguana melanoderma .

Iguana melanoderma is distinguished from all other iguana lineages by the following combination of characteristics. This description is mainly based on adult iguanas observed in the field with the most developed diagnostic characteristics.

Iguana melanoderma belongs to the Common Green Iguana phenotype (in contrast to the Iguana delicatissima phenotype) with its large subtympanic plate, the arrangement of sublabial scales, the rectangular shape of the dewlap, the shape and the distribution of the gular spikes, its flat head, its tubercular nape scales, and its banded tail ( Breuil 2013, 2016). By the absence of horns on the snout, Iguana melanoderma can be distinguished from Iguana rhinolopha and I. iguana insularis , and from I. iguana sanctaluciae (Fig. 7 ).

The most distinctive morphological trait of this new taxon is its general color: adults from Saba and Montserrat iguanas are melanistic. There is a tendency for individuals to become blacker with age (Fig. 8 ).

There is always a black spot between the brown to grey-brown eye and the tympanum. In fully grown adults, the subtympanic plate is 2 to 2.5 times the height of the tympanum. Its color varies from light pink to dark pink with a proportion of black coloration ranging from hardly black to all black. The tympanum can be completely black. The labial and sublabial scales have the same coloring as the subtympanic plate. The lower labial scales, anterior to the subtympanic plate, are arranged in 3-5 pairs of scales of fairly similar size, one in front of the other, and do not form a mosaic of small scales. The head is usually black on the sides (tympanum, eye, subtympanic and posterior labial and sublabial parts), whereas the snout and the top of the head are light to dark grey, and in some individuals these parts are nearly entirely black.

The dewlap is completely black in adults, as in Iguana iguana sanctaluciae (Fig. 7 ). The gular spikes are light to dark grey with a variable portion of black. They are flat, triangular, quite small, and not exceed 10 in number. A variable percentage of the gular scales on the lower part of the dewlap are pentagonal or hexagonal, and do not overlap.

The dorsal parts of the limbs are more or less black, and the black is more developed in older individuals extending over the ventral face of the limb. Some specimens have entirely black head and legs whereas the body is dark green. This body coloration is the result of a black anterior part and a lighter posterior part of most scales while some others are black or dark green. The spikes of the dorsal crest range from light to dark grey; the central part can be black. Some individuals have entirely black dorsal and caudal crests.

The nuptial coloration is present in both sexes, but more vivid and more developed in males than in females. Breeding adults sometimes become reddish-orange over the entire body ( Powell et al. 2005) and the jowls are pinkish if not too melanistic. They never become as orange as I. rhinolopha . According to Lazell (1973), in melanistic individuals, the face, snout, and sometimes the sides are usually purple or brown.

The iguanas from Saba and Montserrat begin their lives with discontinuous light, medium and dark green dorsolateral bands and patches, some of which are underlined by white markings without black on the head and limbs. The black spot between the eye and the tympanum is present in one-year-old individuals, but it is very small and poorly developed. The proportion of the areas covered by these different green markings varies in hatchlings. In juveniles and subadults, this pattern then gradually changes to an ornate arrangement, called a carpet pattern by Lazell (1973) which consists of interrupted bands and patches, green and brown or grey and green, according to the skin shade (Fig. 9 ). This highly disruptive carpet pattern may be the mark of an ancient adaptation to crypsis. A light carpet pattern, with brown and green, is also sometimes present in adults. With age, the individuals become darker, causing the carpet pattern to fade. The granular scales on the body are green, but at their periphery they are black, and a varying proportion of these scales are completely black. The details and chronology of these ontogenetic transformations are unknown.

There are no nasal horns. The tubercular nape scales are numerous, prominent, ranging from light to dark grey, and are often aligned in many rows. The cheek scales usually do not overlap.

Montserrat iguanas are similar to those of Saba. Overall, they appear less melanistic, but some individuals are as black as those of Saba. The head appears to be flatter and more elongated in Montserrat than in Saba, but more data are needed to assess putative morphological divergence between the two populations.

Biology.

In Saba, Iguana melanoderma lives on cliffs (Fig. 10 ), in trees and bushes, in shrublands, and deciduous woodlands. One of the most striking facts about Saba is that these iguanas live in a foggy and cool environment up to about 500 m a.s.l. They sunbathe as soon as the sun rises (Figs 10 , 11 ). The black coloration may be an adaptative trait to help rapidly raise their body temperature in these cool conditions ( Breuil 2013, 2016). Hatchlings were observed in June and July.

In Montserrat, Iguana melanoderma have been reported in a variety of habitats, mostly in coastal residential areas. In 1995, before the eruption of the Soufrière Hills, iguanas could be seen in the then capital, Plymouth, along the seawall defenses just above high tide (M. Morton, personal observation). Blankenship (1990) reported a preference for ghauts (streams), and the majority of records to date are from locations near ghauts or rivers (J. Dawson, SL Adams, pers. comm., E. Corry, pers. obs.).

In Montserrat, there are far fewer records from mesic forest ( Hamilton et al. 2008) from the Centre. The highest elevation for iguana sightings has been cited as ca. 400 m a.s.l. (G. Garcia pers. comm). However, this may reflect a bias towards areas where people spend the most time. Fewer people visit the forests, and far fewer people travel to the east of the island after the eruption. That being said, Daltry (1995) reported a negative association between iguana sightings and the elevation of the study plot (P <0.0023).

According to Blankenship (1990), Montserrat iguanas breed from late February, when nest digging begins, until the emergence of hatchlings in July and August. Clutch sizes range from 15 to 30 ( Blankenship 1990). Observations after 1995, i.e., after the start of the last eruptions cycle of the Soufrière Hills, indicate that nesting has continued at these times of the year; egg-laying was recorded in March and April (E. Corry, M. Morton, personal observations). In April 2008, one female was observed nesting in sand at Iles Bay, an area of recent lahar deposits at the mouth of the Belham River, as well as higher up in this now subterranean stream (E. Corry; M. Morton, personal observations). This is consistent with Blankenship (1990), who stated that they nest in loose soil.

Distribution.

The volcanic island of Montserrat is 102 km2. In 1995, the dormant volcano of the Soufrière Hills became active. Catastrophic eruptions in 1997 rendered two thirds of the south of the island uninhabitable and led to the creation of an exclusion zone (Fig. 12A ). There are three major mountain ranges with natural vegetation restricted to small areas on the tops of two. The highest point before the eruption was Chances Peak, which reached 914 m a.s.l. The subsequent lava dome naturally rises and falls periodically; its maximum height was 1050 m a.s.l. in 2015. According to Lazell (1973), in the 1960s, iguanas were locally abundant in southern Montserrat and were present throughout the lowlands of the island. Steadman et al. (1984) reported that the species occurs in scattered areas around the island, and is locally common in some places along the southern coast. According to Reitz (1994), the iguana was not common on the island.

The island of Saba is about 13 km2 and rises to an altitude of 877 m a.s.l. on Mt Scenery. This peak forms the summit of a dormant 400 ka-year-old volcano ( Roobol and Smith 2004). Saba is surrounded by steep cliffs on all sides. There is no permanent beach for the laying of iguana eggs as in Martinique around Mt Pelée. Much of the central highlands of the island, above 400-500 m, are covered with dense primary and secondary rainforests. Rain and moisture from the surrounding clouds bring humidity to the forest. This pristine habitat thus seems to be incompatible for a permanent presence with the thermal and solar needs of iguanas, even in the canopy where clouds and mist are often present.

The superposition of the geological map ( Roobol and Smith 2004) and the current vegetation shows that the rainforest is developing on the andesite lava of the recent central volcano. On the pelean volcanic domes on the periphery of Mount Scenery, patches of xeric vegetation are found, as on Lower and Upper Hell’s Gate, Level, and Great Hill. Some hills, such as Old Booby, have little tree vegetation; overgrazing by goats is responsible for this. Some of the cliffs are made of volcanic tuff which is a poorly consolidated material that cannot withstand heavy tropical rains and where trees cannot grow. The vegetation and the climatic conditions, temperature and sun, therefore seem to restrict the distribution of iguanas and thus their numbers.

As such, the Saban Black Iguana is mainly present on the Windward side, from sea level to about 500 m a.s.l. (hilltop at the Level 514 m) (Fig. 12B ). The main concentration is found on the slopes of Lower and Upper Hell’s Gate, and on the cliffs of Booby Hill. The total range of this taxon is about 5-6 km2. There are also some iguanas at The Bottom. This locality is located west of Windwardside village, but not in the shadow of Mt Scenery. For Lazell (1973), in the 1960s, Saba iguanas were common everywhere, even at 800 m a.s.l. in the rainforest of Mt Scenery.

Figures

Figure 1. Geographical distribution of the three iguana groups identified by Lazell (1973) in the 1960 s and new taxonomic proposition. In the 1960 s, the invasive iguanas from South America (Iguana iguana) were only present in the iles des Saintes and Guadeloupe (Basse-Terre) and formed the Central Group. Now, alien iguanas are present and breed on every bank (van den Burg et al. 2018 b). The southern group is now considered to support two subspecies Iguana iguana insularis and Iguana iguana sanctaluciae (Breuil et al. 2019). The northern group is considered here as a new species.

Figure 5. Holotype of Iguana melanoderma sp. nov. A Dorsal view B lateral view C dorsal view of the head D lateral view of the head. MCZ R- 75832 from Saba, Windwardside. Museum of Comparative Zoology, Harvard University. President and Fellows of Harvard College. 1. Black patch between the tympanum and the subtympanic plate. 2. High number of aligned nape tubercles. 3. No horns on the stout. 4. Dorsal carpet pattern. 5. Black on the upper part of the forelimb. 6. Prominent nostrils. 7. Anterior part of the snout, not black. 8. Subtympanic plate with a dark posterior patch. 9. Black anterior edge of lower sublabial scales. 10. Fewer than 10 triangular gular spikes extended in the upper part of the lower dewlap. 11. Entirely black dewlap.

Figure 6. Paratype of Iguana melanoderma sp. nov. A Left side view of the head B right side view of the head. MCZ R 126377 from Montserrat, Old Road Bluff. Museum of Comparative Zoology, Harvard University. President and Fellows of Harvard College. 1. Black patch between the tympanum and the subtympanic plate. 2. High number of aligned nape tubercles. 3. No horns on the stout. 5. Black spot on the upper forelimb. 6. Prominent nostrils. 7. Anterior part of the snout, not black. 8. Subtympanic plate with a dark posterior patch. 9. Black anterior edge of lower sublabial scales. 10. Fewer than 10 triangular gular spikes extended in the upper part of the lower part of the dewlap. 11. Dewlap entirely black. 12. Lower sublabial scales arranged in pairs of nearly the same size.

Figure 7. Comparison of morphological features of the head. A Young adult male. 1. Subtympanic plate with pink in the center. 2. Lower sublabial scales arranged in pairs of nearly identical size. 3. Black anterior edge of the lower sublabial scales. 4. Black border around the subtympanic plate. 5. Prominent nostrils. 6. Black spot between the eye and the tympanum. 7. Absence of horn and light snout. 8. Dark brown eye. 9. Triangular gular spikes. 10. Fewer than 10 gular spikes extended in the upper part of the lower dewlap. 11. High number of aligned nape tubercles. 12. Prominent light-grey tubercles. 13. Light greyish-green coloration on the neck. 14. High light-grey dorsal spines. 15. Dewlap half black. 16. Dorsal part of the limb with light-green scales becoming black with the extension of melanin from the anterior edge to the posterior edge of the scales. B Old male of Iguana melanoderma (Saba). 1. Large all-black subtympanic plate. 2. Extension of the black pigment on the sublabial scales. 3. Black coloration of the labial and upper sublabial scales. 4. Black coloration between the tympanum and the subtympanic plate. 6. Extension of the black spot around the eye and on the posterior labial and sublabial scales. 7. Snout turning dark grey. 9, 10. Gular spikes turning dark grey with extension of black patches. 12. Dark grey nape tubercles. 13. Black coloration on the neck. 14. Dorsal spikes turning black. 15. Dewlap completely black. 16. Black upper face of the limb.

Figure 8. The dorsal carpet pattern of young adults Iguana melanoderma. A Montserrat B Saba. The dorsal coloration is formed by darker more or less interrupted dorso-ventral bands (brown, dark grey) on a lighter ground. This pattern disappears in old individuals. The black patch between the eye and the tympanum is already visible.

Figure 9. A Old adult from Montserrat B old adult from Saba. In these old individuals the carpet pattern is absent. The head is almost entirely black, except for the top and the snout. The dewlap, neck, dorsal spikes, and forelimb are black. Dorsal and lateral coloring is more variable, ranging from entirely black to a mosaic of black, brown, and dark green scales.

Figure 10. Iguana melanoderma sunbathing at dawn on the Windward coast of Saba.

Figure 11. A basking Iguana melanoderma optimizing after different trials its warming by a curved position when the sun is low on the horizon on the Windward coast of Saba.

Figure 12. Distribution of Iguana melanoderma in Montserrat and Saba. Each square is 2 km along a side.